Exercise-induced bronchoconstriction in elite athletes: a narrative review

References

• Parsons JP, Hallstrand TS, Mastronarde JG, et al. An official American Thoracic Society clinical practice guideline: exercise-induced bronchoconstriction. Am J Respir Crit Care Med. 2013;187:1016–1027.
   PubMed Web of Science ®Google Scholar
• Gawlik R, Kurowski M, Kowalski M, et al. Asthma and exercise-induced respiratory disorders in athletes. The position paper of the polish society of allergology and polish society of sports medicine. Postepy Dermatol Alergol. 2019;36:1.
   PubMed Web of Science ®Google Scholar
• Bonini M, Gramiccioni C, Fioretti D, et al. Asthma, allergy and the Olympics: a 12-year survey in elite athletes. Curr Opin Allergy Clin Immunol. 2015;15:184–192.
   PubMed Web of Science ®Google Scholar
• Koya T, Ueno H, Hasegawa T, et al. Management of exercise-induced bronchoconstriction in athletes. J Allergy Clin Immunol Pract. 2020;8:2183–2192.
   PubMed Web of Science ®Google Scholar
• Price OJ, Hull JH. Asthma in elite athletes: who cares? Clin Pulm Med. 2014;21:68–75.
   Google Scholar
• Price OJ, Sewry N, Schwellnus M, et al. Prevalence of lower airway dysfunction in athletes: a systematic review and meta-analysis by a subgroup of the IOC consensus group on ‘acute respiratory illness in the athlete.’ Br J Sports Med. 2022;56:213–222.
   PubMed Web of Science ®Google Scholar
• Aggarwal B, Mulgirigama A, Berend N. Exercise-induced bronchoconstriction: prevalence, pathophysiology, patient impact, diagnosis and management. NPJ Prim Care Respir Med. 2018;28:1–8.
   PubMed Web of Science ®Google Scholar
• Parsons JP, Craig TJ, Stoloff SW, et al. Impact of exercise-related respiratory symptoms in adults with asthma: exercise-induced bronchospasm landmark national survey. Allergy Asthma Proc. 2011;32:431–437.
   PubMed Web of Science ®Google Scholar
• Rundell KW, Anderson SD, Sue‐Chu M, et al. Air quality and temperature effects on exercise‐induced bronchoconstriction. Compr Physiol. 2011;5:579–610.
   Google Scholar
• Del Giacco SR, Firinu D, Bjermer L, et al. Exercise and asthma: an overview. Eur Clin Respir J. 2015;2:27984.
   PubMed Web of Science ®Google Scholar
• Atchley TJ, Smith DM. Exercise-induced bronchoconstriction in elite or endurance athletes: pathogenesis and diagnostic considerations. Ann Allergy Asthma Immunol. 2020;125:47–54.
   PubMed Web of Science ®Google Scholar
• Carlsen KH. Sports in extreme conditions: the impact of exercise in cold temperatures on asthma and bronchial hyper-responsiveness in athletes. Br J Sports Med. 2012;46:796–799.
   PubMed Web of Science ®Google Scholar
• Mountjoy M, Fitch K, Boulet LP, et al. Prevalence and characteristics of asthma in the aquatic disciplines. J Allergy Clin Immunol. 2015;136:588–594.
   PubMed Web of Science ®Google Scholar
• Anderson SD. Is there a unifying hypothesis for exerciseinduced asthma? J Allergy Clin Immunol. 1984;73:660–665.
   PubMed Web of Science ®Google Scholar
• Eggleston PA, Kagey-sobotka A, Schleimer RP, et al. Interaction between hyperosmolar and IgE-mediated histamine release from basophils and mast cells. Am Rev Respir Dis. 1984;130:86–91.
   PubMed Web of Science ®Google Scholar
• Brannan JD, Koskela H, Anderson SD, et al. Responsiveness to mannitol in asthmatic subjects with exercise and hyperventilation-induced asthma. Am J Respir Crit Care Med. 1998;158:1120–1126.
   PubMed Web of Science ®Google Scholar
• Irewall T, Söderström L, Lindberg A, et al. High incidence rate of asthma among elite endurance athletes: a prospective 4-year survey. J Asthma. 2021;58:735–741.
   PubMed Web of Science ®Google Scholar
• Bolger C, Tufvesson E, Anderson SD, et al. Effect of inspired air conditions on exercise-induced bronchoconstriction and urinary CC16 levels in athletes. J Appl Physiol. 2011;111:1059–1065.
   PubMed Web of Science ®Google Scholar
• Correia Junior MAV, Costa EC, Sarinho SW, et al. Exercise-induced bronchospasm in a hot and dry region: study of asthmatic, rhinitistic and asymptomatic adolescents. Expert Rev Respir Med. 2017;11:1013–1019.
   PubMed Web of Science ®Google Scholar
• Evans TM, Rundell KW, Beck KC, et al. Cold air inhalation does not affect the severity of EIB after exercise or eucapnic voluntary hyperventilation. Med Sci Sports Exerc. 2005;37:544–549.
   PubMed Web of Science ®Google Scholar
• Rundell KW, Sue-Chu M. Air quality and exercise-induced bronchoconstriction in elite athletes. Immunol Allergy Clin North Am. 2013;33:409–421.
   PubMed Web of Science ®Google Scholar
• Cox A, Sleeth D, Handy R, et al. Characterization of CO and NO2 exposures of ice skating rink maintenance workers. J Occup Environ Hyg. 2019;16:101–108.
   PubMed Web of Science ®Google Scholar
• Nordberg GF, Lundstrom NG, Forsberg B, et al. Lung function in volunteers before and after exposure to trichloramine in indoor pool environments and asthma in a cohort of pool workers. BMJ open. 2012;2:e000973.
   PubMed Web of Science ®Google Scholar
• Carter RAA, Allard S, Croué JP, et al. 500 days of swimmers: the chemical water quality of swimming pool waters from the beginning. Environ Sci Pollut Res Int. 2019;26:29110–29126.
   PubMed Web of Science ®Google Scholar
• Eriksson LM, Irewall T, Lindberg A, et al. Prevalence, age at onset, and risk factors of self‐reported asthma among Swedish adolescent elite cross‐country skiers. Scand J Med Sci Sports. 2018;28:180–186.
   PubMed Web of Science ®Google Scholar
• Anderson SD, Kippelen P. Airway injury as a mechanism for exercise-induced bronchoconstriction in elite athletes. J Allergy Clin Immunol. 2008;122:225–235.
   PubMed Web of Science ®Google Scholar
• Sacha JJ, Quinn JM. The environment, the airway, and the athlete. Ann Allergy Asthma Immunol. 2011;106:81–87.
   PubMed Web of Science ®Google Scholar
• Couillard S, Bougault V, Turmel J, et al. Perception of bronchoconstriction following methacholine and eucapnic voluntary hyperpnea challenges in elite athletes. Chest. 2014;145:794–802.
   PubMed Web of Science ®Google Scholar
• Martin TR, Castile RG, Fredberg JJ, et al. Airway size is related to sex but not lung size in normal adults. J Appl Physiol. (1985) 1987;63:2042–2047.
   Web of Science ®Google Scholar
• Hoffstein V. Relationship between lung volume, maximal expiratory flow, forced expiratory volume in one second, and tracheal area in normal men and women. Am Rev Respir Dis. 1986;134:956–961.
   PubMed Web of Science ®Google Scholar
• Sheel AW, Guenette JA. Mechanics of breathing during exercise in men and women: sex versus body size differences? Exerc Sport Sci Rev. 2008;36:128–134.
   PubMed Web of Science ®Google Scholar
• Harms CA. Does gender affect pulmonary function and exercise capacity? Respir Physiol Neurobiol. 2006;151:124–131.
   PubMed Web of Science ®Google Scholar
• Baldaçara RPC, Silva I. Association between asthma and female sex hormones. Sao Paulo Med J. 2017;135:04–14.
   PubMed Web of Science ®Google Scholar
• Kippelen P, Fitch KD, Anderson SD, et al. Respiratory health of elite athletes–preventing airway injury: a critical review. Br J Sports Med. 2012;46:471–476.
   PubMed Web of Science ®Google Scholar
• Carbonnelle S, Bernard A, Doyle I, et al. Fractional exhaled NO and serum pneumoproteins after swimming in a chlorinated pool. Med Sci Sports Exerc. 2008;40:1472.
   PubMed Web of Science ®Google Scholar
• Rundell KW, Caviston R, Hollenbach AM, et al. Vehicular air pollution, playgrounds, and youth athletic fields[J]. Inhal Toxicol. 2006;18(8):541–547.
   PubMed Web of Science ®Google Scholar
• Kennedy MD, Steele AR, Parent EC, et al. Cold air exercise screening for exercise induced bronchoconstriction in cold weather athletes. Respir Physiol Neurobiol. 2019;269:103262.
   PubMed Web of Science ®Google Scholar
• Hanstock HG, Ainegren M, Stenfors N. Exercise in sub-zero temperatures and airway health: implications for athletes with special focus on heat-and-moisture-exchanging breathing devices. Front Sports Act Living. 2020;2:34.
   PubMedGoogle Scholar
• Frischhut C, Kennedy MD, Niedermeier M, et al. Effects of a heat and moisture exchanger on respiratory function and symptoms post–cold air exercise. Scand J Med Sci Sports. 2020;30:591–601.
   PubMed Web of Science ®Google Scholar
• Jackson AR, Hull JH, Hopker JG, et al. The impact of a heat and moisture exchange mask on respiratory symptoms and airway response to exercise in asthma. ERJ Open Res. 2020;6. DOI:10.1183/23120541.00271-2019.
   Google Scholar
• Stenfors N, Hanstock H, Ainegren M, et al. Usage of and attitudes toward heat‐and moisture‐exchanging breathing devices among adolescent skiers. Transl Sports Med. 2021;4:337–343.
   Google Scholar
• Tutt AS, Persson H, Andersson EP, et al. A heat and moisture-exchanging mask impairs self-paced maximal running performance in a sub-zero environment. Eur J Appl Physiol. 2021;121:1979–1992.
   PubMed Web of Science ®Google Scholar
• Mickleborough TD, Lindley MR, Turner LA. Comparative effects of a high-intensity interval warm-up and salbutamol on the bronchoconstrictor response to exercise in asthmatic athletes. Int J Sports Med. 2007;28:456–462.
   PubMed Web of Science ®Google Scholar
• Elkins MR, Brannan JD. Warm-up exercise can reduce exercise-induced bronchoconstriction. Br J Sports Med. 2013;47:657–658.
   PubMed Web of Science ®Google Scholar
• Stickland MK, Rowe BH, Spooner CH, et al. Effect of warm-up exercise on exercise-induced bronchoconstriction. Med Sci Sports Exerc. 2012;44:383–391.
   PubMed Web of Science ®Google Scholar
• Eichenberger PA, Scherer TA, Spengler CM. Pre-exercise hyperpnea attenuates exercise-induced bronchoconstriction without affecting performance. PloS One. 2016;11:e0167318.
   PubMed Web of Science ®Google Scholar
• Kleniewska P, Pawliczak R. The participation of oxidative stress in the pathogenesis of bronchial asthma. Biomed Pharmacother. 2017;94:100–108.
   PubMed Web of Science ®Google Scholar
• Gomes EC, Stone V, Florida-James G. Impact of heat and pollution on oxidative stress and CC16 secretion after 8 km run. Eur J Appl Physiol. 2011;111:2089–2097.
   PubMed Web of Science ®Google Scholar
• Hemilä H. Vitamin C may alleviate exercise-induced bronchoconstriction: a meta-analysis. BMJ open. 2013;3:e002416.
   PubMed Web of Science ®Google Scholar
• Tecklenburg SL, Mickleborough TD, Fly AD, et al. Ascorbic acid supplementation attenuates exercise-induced bronchoconstriction in patients with asthma. Respir Med. 2007;101:1770–1778.
   PubMed Web of Science ®Google Scholar
• Mickleborough TD, Lindley MR, Ray S. Dietary salt, airway inflammation, and diffusion capacity in exercise-induced asthma. Med Sci Sports Exerc. 2005;37:904–914.
   PubMed Web of Science ®Google Scholar
• Mickleborough TD, Lindley MR, Ionescu AA, et al. Protective effect of fish oil supplementation on exercise-induced bronchoconstriction in asthma. Chest. 2006;129:39–49.
   PubMed Web of Science ®Google Scholar
• Neuman I, Nahum H, Ben‐Amotz A. Reduction of exercise‐induced asthma oxidative stress by lycopene, a natural antioxidant. Allergy. 2000;55:1184–1189.
   PubMed Web of Science ®Google Scholar
• McLoughlin R, Berthon BS, Rogers GB, et al. Soluble fibre supplementation with and without a probiotic in adults with asthma: a 7-day randomised, double blind, three way cross-over tria. EBioMedicine. 2019;46:473–485.
   PubMed Web of Science ®Google Scholar
• Rundell KW, Im J, Mayers LB, et al. Self-reported symptoms and exercise-induced asthma in the elite athlete. Sports Med Health Sci. 2001;33:208–213.
   Google Scholar
• Allen H, Hull J, Backhouse SH, et al. The allergy questionnaire for athletes provides value in ruling-out exercise-induced bronchoconstriction. Allergy. 2019;126:681–690.
   Google Scholar
• Allen H, Backhouse SH, Hull JH, et al. Anti-doping policy, therapeutic use exemption and medication use in athletes with asthma: a narrative review and critical appraisal of current regulations. Sports Med. 2019;49:659–668.
   PubMed Web of Science ®Google Scholar
• Hull JH, Burns P, Carre J, et al. BTS clinical statement for the assessment and management of respiratory problems in athletic individuals. Thorax. 2022;77:540–551.
   PubMed Web of Science ®Google Scholar
• Hammer IJ, Halvorsen T, Vollsæter M, et al. Conundrums in the breathless athlete; exercise induced laryngeal obstruction or asthma? Scand J Med Sci Sports. 2022;42:1041–1049.
   Web of Science ®Google Scholar
• Brennan FH Jr, Alent J, Ross MJ. Evaluating the athlete with suspected exercise-induced asthma or bronchospasm. Curr Sports Med Rep. 2018;17:85–89.
   PubMed Web of Science ®Google Scholar
• Greiwe J, Cooke A, Nanda A, et al. Work group report: perspectives in diagnosis and management of exercise-induced bronchoconstriction in athletes. J Allergy Clin Immunol Pract. 2020;8:2542–2555.
   PubMed Web of Science ®Google Scholar
• Pigakis KM, Stavrou VT, Pantazopoulos I, et al. Exercise-induced bronchospasm in elite athletes. Cureus. 2022;14:e20898.
   PubMed Web of Science ®Google Scholar
• Rundell KW, Slee JB. Exercise and other indirect challenges to demonstrate asthma or exercise-induced bronchoconstriction in athletes. J Allergy Clin Immunol. 2008;122:238–246.
   PubMed Web of Science ®Google Scholar
• Holzer K, Anderson SD, Douglass J. Exercise in elite summer athletes: challenges for diagnosis. J Allergy Clin Immunol. 2002;110:374–380.
   PubMed Web of Science ®Google Scholar
• Rundell KW, Wilber RL, Szmedra L, et al. Exercise-induced asthma screening of elite athletes: field versus laboratory exercise challenge. Med Sci Sports Exerc. 2000;32:309–316.
   PubMed Web of Science ®Google Scholar
• Weiler JM, Brannan JD, Randolph CC, et al. Exercise-induced bronchoconstriction update—2016. J Allergy Clin Immunol. 2016;138:1292–1295. e36.
   PubMed Web of Science ®Google Scholar
• Hull JH, Ansley L, Price OJ, et al. Eucapnic voluntary hyperpnea: gold standard for diagnosing exercise-induced bronchoconstriction in athletes? Sports Med. 2016;46:1083–1093.
   PubMed Web of Science ®Google Scholar
• Anderson SD, Argyros GJ, Magnussen H, et al. Provocation by eucapnic voluntary hyperpnoea to identify exercise induced bronchoconstriction. Br J Sports Med. 2001;35:344–347.
   PubMed Web of Science ®Google Scholar
• Holzer K, Douglass JA. Exercise induced bronchoconstriction in elite athletes: measuring the fall. Thorax. 2006;61:94–96.
   PubMed Web of Science ®Google Scholar
• Stickland MK, Rowe BH, Spooner CH, et al. Accuracy of eucapnic hyperpnea or mannitol to diagnose exercise-induced bronchoconstriction: a systematic review. Ann Allergy Asthma Immunol. 2011;107:229–234. e8.
   PubMed Web of Science ®Google Scholar
• Voutilainen M, Malmberg LP, Vasankari T, et al. Exhaled nitric oxide indicates poorly athlete’s asthma. Clin Respir J. 2013;7:347–353.
   PubMed Web of Science ®Google Scholar
• Ersson K, Johansson H, Mallmin E, et al. Exercise-induced bronchoconstriction (EIB) is not associated with exhaled nitric oxide (FeNO) in adolescent athletes. Eur Respir J. 2019;54:PA4508.
   Web of Science ®Google Scholar
• Evans TM, Rundell KW, Beck KC, et al. Impulse oscillometry is sensitive to bronchoconstriction after eucapnic voluntary hyperventilation or exercise. J Asthma. 2006;43:49–55.
   PubMed Web of Science ®Google Scholar
• Price OJ, Ansley L, Bikov A, et al. The role of impulse oscillometry in detecting airway dysfunction in athletes. J Asthma. 2016;53:62–68.
   PubMed Web of Science ®Google Scholar
• Sekiyama A, Gon Y, Terakado M, et al. Glucocorticoids enhance airway epithelial barrier integrity. Int Immunopharmacol. 2012;12:350–357.
   PubMed Web of Science ®Google Scholar
• Koh MS, Tee A, Lasserson TJ, et al. Inhaled corticosteroids compared to placebo for prevention of exercise induced bronchoconstriction. Cochrane Database Syst Rev. 2007;3:CD002739.
   Google Scholar
• Jackson AR, Hull JH, Hopker JG, et al. Impact of detecting and treating exercise-induced bronchoconstriction in elite footballers. ERJ Open Res. 2018;4:00122–2017.
   PubMedGoogle Scholar
• Hancox RJ, Subbarao P, Kamada D, et al. β2-agonist tolerance and exercise-induced bronchospasm. Am J Respir Crit Care Med. 2002;165:1068–1070.
   PubMed Web of Science ®Google Scholar
• Bonini M, Hull JH. Pharmacological treatment of asthma-related issues in athletes. Complete Guide Respir Care Athletes. 1st Edition. 2020;75–85:9780429492341.
   Google Scholar
• Colice G, Calhoun WJ. Section 2. Exercise-induced bronchospasm: albuterol versus montelukast: highlights of the Asthma Summit 2009: beyond the guidelines. World Allergy Organ J. 2010;3:23–30.
   PubMedGoogle Scholar
• Anhuai Y, Jinzhong C. Research progress of exercise-induced asthma. Hainan Med J. 2021;32:1885–1889.
   Google Scholar
• [cited 2022 Jan 2]. Available from: https://www.chinada.cn/upload/files/2021/12/4f311ac13aa8de24.pdf
   Google Scholar
• Allen H, Price OJ, Hull JH, et al. Asthma medication in athletes: a qualitative investigation of adherence, avoidance and misuse in competitive sport. J Asthma. 2022;59:811–822.
   PubMed Web of Science ®Google Scholar
• Hull JH, Hull PJ, Parsons JP, et al. Approach to the diagnosis and management of suspected exercise-induced bronchoconstriction by primary care physicians. BMC Pulm Med. 2009;9:1–7.
   PubMedGoogle Scholar
• Mottram D, Chester N, Atkinson G, et al. Athletes’knowledge and views on OTC medication. Int J Sports Med. 2008;29:851–855.
   PubMed Web of Science ®Google Scholar
• Dickinson JW, Whyte GP, McConnell AK, et al. Impact of changes in the IOC-MC asthma criteria: a British perspective. Thorax. 2005;60:629–632.
   PubMed Web of Science ®Google Scholar
• Pluim BM, de Hon O, Staal JB, et al. β2-Agonists and physical performance. Sports Med. 2011;41:39–57.
   PubMed Web of Science ®Google Scholar
• [cited 2021 Oct 6]. Available from: https://www.wada-ama.org/en/media/news/2016-09/wada-confirms-attack-by-russian-cyber-espionage-group
   Google Scholar
• Riiser A, Stensrud T, Stang J, et al. Can β2-agonists have an ergogenic effect on strength, sprint or power performance? Systematic review and meta-analysis of RCTs. Br J Sports Med. 2020;54:1351–1359.
   PubMed Web of Science ®Google Scholar
• [cited 2021 Oct 8]. Available from: https://www.theguardian.com/sport/2016/oct/14/marcel-kittel-cyclists-severe-asthma-paralympics
   Google Scholar
• Bourdon F, Schoch L, Broers B, et al. French speaking athletes’ experience and perception regarding the whereabouts reporting system and therapeutic use exemptions. Perform Enhanc Health. 2014;3:153–158.
   Google Scholar
• Hull JH, Pavord ID. Treating asthma exacerbations in athletes: TUE or not TUE? Lancet Respir Med. 2018;6:8–10.
   PubMed Web of Science ®Google Scholar
• Overbye M, Wagner U. Between medical treatment and performance enhancement: an investigation of how elite athletes experience therapeutic use exemptions. Int J Drug Policy. 2013;24:579–588.
   PubMed Web of Science ®Google Scholar
• Fitch K. Glucocorticoids at the Olympic Games: state-of-the-art review. Br J Sports Med. 2016;50:1267.
   PubMed Web of Science ®Google Scholar
• [cited 2021 Oct 10]. Available from: https://www.wada-ama.org/sites/default/files/resources/files/WADA_IOC_Report_Olympic_Games_2000.pdf
   Google Scholar
• [cited 2021 Oct 10]. Available from: https://www.wada-ama.org/sites/default/files/resources/files/WADA_Prohibited_List_2004_EN.pdf
   Google Scholar
• [cited 2021 Oct 11]. Available from: https://www.wada-ama.org/sites/default/files/resources/files/WADA_Summary_of_Modifications_2009_EN.pdf
   Google Scholar
• [cited 2021 Oct 11]. Available from: https://www.wada-ama.org/sites/default/files/resources/files/asthma_version_7.0_december_2020.pdf
   Google Scholar